Elsevier

Medical Hypotheses

Volume 77, Issue 3, September 2011, Pages 339-344
Medical Hypotheses

Biodiversity and leptospirosis risk: A case of pathogen regulation?

https://doi.org/10.1016/j.mehy.2011.05.009Get rights and content

Abstract

Well balanced ecosystems have an essential role in disease regulation, and consequently their correct functioning is increasingly recognised as imperative for maintaining human health. Disruptions to ecosystems have been found to increase the risk of several diseases, including Hantavirus, Lyme disease, Ross River virus, malaria and Ciguatera fish poisoning. Leptospirosis is a globally important emerging zoonosis, caused by spirochaete bacteria, borne by many mammalian hosts, and also transmitted environmentally. We propose that leptospirosis incidence in humans is also linked to ecosystem disruption, and that reduced biodiversity (the diversity of species within an ecological community) may be associated with increased leptospirosis incidence. To investigate this hypothesis, the relationship between biodiversity levels of island nations and their annual leptospirosis incidence rates (adjusted for GDP per capita) was examined by linear correlation and regression. Supportive, statistically significant negative associations were obtained between leptospirosis incidence and (a) total number of species (r2 = 0.69, p < 0.001) and (b) number of mammal species (r2 = 0.80, p < 0.001) in univariate analysis. In multivariable analysis only the number of mammal species remained significantly associated (r2 = 0.81, p = 0.007). An association between biodiversity and reduced leptospirosis risk, if supported by further research, would emphasise the importance of managing the emergence of leptospirosis (and other infectious diseases) at a broader, ecosystem level.

Introduction

Ecosystems have been recognised as providers of life-sustaining and otherwise beneficial services for human populations, including provisioning, cultural, supporting and regulating services [1], [2]. With regards to disease regulation as an ecosystem service, it is commonly accepted that as biodiversity declines, biological control systems that suppress the emergence and proliferation of pest and pathogen species are disrupted [3], and that the dynamic equilibrium among species and functional groups they form is therefore necessary to safeguard human health [4]. Disruptions to ecosystems have been found to increase the risk of several animal borne diseases, including Hantavirus [5], Lyme disease [6], Ross River virus [7], malaria [2] and Ciguatera fish poisoning [8]. Two principal mechanisms by which biodiversity can be protective of human health through regulation of infectious diseases are proposed in the literature: firstly, regulation of pathogen host populations by direct predatory and competitive interactions, and secondly, reduction of pathogen success by the dilution effect. A biodiverse community has a greater probability of supporting predatory species which effectively regulate prey populations [5], [9], thereby reducing pathogen levels if the prey species is a host. Similarly, a larger number of species within a community makes the presence of competitors more likely [10], which will lower a host population’s growth or survival rates [5]. The dilution effect operates when a finite number of pathogens or transmission events (e.g. mosquito bites) are distributed amongst two or more host species, where one of these species is a less competent host, thus reducing pathogen proliferation and disease risk. Alternatively, the dilution effect may refer to the reduction in host–host interactions by the presence of other species, reducing transmission opportunities for the pathogen [11]. More generally, higher biodiversity is arguably correlated with ecosystem stability, i.e. its ability to resist and recover from change caused by external disturbances, including the invasion of exotic species which may act as pathogen hosts or reservoirs [12], [13]. In such a case, greater species diversity reduces the probability of any one pathogen host becoming dominant within the system.

Leptospirosis, the most common of bacterial zoonoses, has been identified as an important emerging global public health problem [14]. With outbreaks common in both developing and developed nations, an estimated 300,000–500,000 severe cases occur per year world-wide [15], and up to 20–30% are fatal [16]. Tropical regions are characterised by higher incidence rates of 10/100,000 people per year, though temperate countries nonetheless commonly report rates of 0.1/100,000 per year [16]. The causative organisms are spirochaetes of the Leptospira genus, with eight pathogenic species divided into over 200 serovars [17]. Leptospires colonise the renal tubules of mammalian reservoir hosts and are chronically shed into urine, thus direct contact with animal tissue or urine can lead to infection in humans [18]. In addition, bacteria persist within the external environment, making exposure to contaminated water or soil major risk factors [19], [20]. Specific serovars are typically associated with different mammalian maintenance reservoirs, which commonly include rats, pigs, cattle, dogs, horses, marsupials and bats [16], [21].

The zoologically and environmentally implicated transmission ecology of leptospirosis begs the question of whether this disease provides another quantifiable link between ecosystem functioning and human health. Muul ([22], p. 1275) points out that “failure to make adequate use of ecological data pertaining to wild hosts species in epidemiological studies of zoonotic disease can be a significant oversight”. While the importance of mammals in the transmission of leptospirosis is certainly recognised, there appear to be no current studies relating ecosystem function or biodiversity mediated regulation to leptospirosis risk or incidence, as there are with rodent-borne haemorrhagic fevers [5], Lyme disease [6] and Ross River virus [7]. The importance of developing a more comprehensive and integrated understanding of large scale mechanisms and determinants of leptospirosis has been identified [23].

Here, we propose that biodiversity (the diversity of species within an ecological community), a major component of ecosystem function, may act to reduce leptospirosis risk and incidence in human populations. Bioregulatory and dilution effects would be expected to act largely on wild hosts such as rats (e.g. Rattus rattus and Rattus norvegicus) rather than on domestic reservoirs. Rats are known to be ecological generalists and prolific invaders, thriving in both wild and peridomestic environments [24]. Importantly, they are frequently the most common source of laboratory confirmed human leptospirosis cases, as indicated by the high prevalence of the icterohaemorrhagiae serovar, mainly carried by rodents [20], [25], [26], [27], [28], [29].

To investigate the hypothesis that biodiversity may regulate leptospirosis incidence, the relationship between biodiversity levels of island nations and their annual leptospirosis incidence rates was examined by correlation and regression. Islands were used in this study for several reasons; many of the world’s island nations are developing nations and found within tropical latitudes, thus are at increased risk of leptospirosis. Islands have also been profoundly affected by rat invasions [24]. Furthermore, islands represent discrete, isolated ecosystems, having been used as natural experimental units in ecological studies since Charles Darwin’s time [30], [31]. Island area and isolation provide approximate measures of biodiversity within themselves [30]. Elucidating causal relationships between ecological factors and disease emergence is typically challenging due to the complexity and non-linear nature of systems involved [32]. Whilst association does not necessarily signify causality, it provides the first step towards evaluating the possible relationship between leptospirosis and biodiversity by the mechanisms described.

Section snippets

Methods

To correlate both direct and indirect measures of biodiversity with leptospirosis incidence, we obtained the following data.

Annual leptospirosis incidence rates for island nations were obtained from published epidemiological literature; usually the number of laboratory confirmed clinical cases reported to public health surveillance systems. Where multiple incidence rates were reported for a single country, the highest quality study was selected. Criteria used to assess study quality were: (1)

Results

Significant negative correlations were observed between leptospirosis incidence and both total species richness and terrestrial mammal species richness, however, leptospirosis incidence rates were not correlated with the indirect biodiversity measure of LMI (Table 1).

As total species richness and terrestrial mammal species richness were significantly correlated with leptospirosis incidence, we examined the untransformed data for these variables. Table 2 lists average annual leptospirosis

Discussion

Our results support the existence of an inverse relationship between biodiversity and leptospirosis incidence on the island nations considered here. Moreover, this study has been useful in identifying terrestrial mammalian species richness as the specific component of biodiversity which appears most strongly associated with leptospirosis incidence. The total number of species and number of terrestrial mammals remained significantly associated with leptospirosis incidence rates after adjusting

Conclusion

This study supports the hypothesis that biodiversity has a bioregulatory effect on leptospirosis incidence. The significant negative relationship between terrestrial mammalian species richness and leptospirosis is consistent with previously supported biological mechanisms and invites further investigation. If this association was validated by the use of higher resolution data, evaluating its causality would require temporal studies, where changes in leptospirosis incidence could be related to a

Grant support

None.

Conflict of interest

None declared.

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